The CRISPR-associated gene cas2 of Legionella pneumophila is required for intracellular infection of amoebae

mBio

Volumn 4, Issue 2, 2013, Pages

  Gunderson, Felizza F ^a   Cianciotto, Nicholas P ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACANTHAMOEBA; AMOEBA (GENUS); ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM MUTANT; CAS1 GENE; CAS2 GENE; CAS4 GENE; CAS9 GENE; CLUSTERED REGULARLY INTERSPACED PALINDROMIC REPEATS; CONTROLLED STUDY; EXTRACELLULAR SPACE; GENE EXPRESSION; GENE LOCUS; GENE STRUCTURE; HARTMANNELLA; HOST CELL; INTRACELLULAR BACTERIUM; LEGIONELLA PNEUMOPHILA; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; CELL LINE; CULTURE MEDIUM; GENE DELETION; GENE EXPRESSION PROFILING; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY;

BACTERIAL DNA; VIRULENCE FACTOR;

ACANTHAMOEBA; CELL LINE; CULTURE MEDIA; DNA, BACTERIAL; GENE DELETION; GENE EXPRESSION PROFILING; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; HARTMANNELLA; HUMANS; LEGIONELLA PNEUMOPHILA; MACROPHAGES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIRULENCE FACTORS;

EID: 84880074536     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00074-13     Document Type: Article

References (105)

1. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8:172
2. Jansen R, Embden JD, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:1565-1575
3. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV. 2011. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9:467-477
4. Mojica FJ, Díez-Villaseñor C, Soria E, Juez G. 2000. Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol. Microbiol. 36:244-246
5. Rezzonico F, Smits TH, Duffy B. 2011. Diversity, evolution, and functionality of clustered regularly interspaced short palindromic repeat (CRISPR) regions in the fire blight pathogen Erwinia amylovora. Appl. Environ. Microbiol. 77:3819-3829
6. Touchon M, Charpentier S, Clermont O, Rocha EP, Denamur E, Branger C. 2011. CRISPR distribution within the Escherichia coli species is not suggestive of immunity-associated diversifying selection. J. Bacteriol. 193:2460-2467
7. Cady KC, White AS, Hammond JH, Abendroth MD, Karthikeyan RS, Lalitha P, Zegans ME, O'Toole GA. 2011. Prevalence, conservation and functional analysis of Yersinia and Escherichia CRISPR regions in clinical Pseudomonas aeruginosa isolates. Microbiology 157:430-437
8. Fricke WF, Mammel MK, McDermott PF, Tartera C, White DG, Leclerc JE, Ravel J, Cebula TA. 2011. Comparative genomics of 28 Salmonella enterica isolates: evidence for CRISPR-mediated adaptive sublineage evolution. J. Bacteriol. 193:3556-3568
9. Berg Miller ME, Yeoman CJ, Chia N, Tringe SG, Angly FE, Edwards RA, Flint HJ, Lamed R, Bayer EA, White BA. 2012. Phage-bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome. Environ. Microbiol. 14:207-227
10. Garrett RA, Vestergaard G, Shah SA. 2011. Archaeal CRISPR-based immune systems: exchangeable functional modules. Trends Microbiol. 19:549-556
11. Bhaya D, Davison M, Barrangou R. 2011. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45:273-297
12. Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP, Dickman MJ, Makarova KS, Koonin EV, van der Oost J. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321: 960-964
13. Lillestøl RK, Redder P, Garrett RA, Brügger K. 2006. A putative viral defence mechanism in archaeal cells. Archaea 2:59-72
14. Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H, Drungowski M, Elge T, Brosius J, Hüttenhofer A. 2002. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc. Natl. Acad. Sci. U. S. A. 99:7536-7541
15. Makarova KS, Aravind L, Wolf YI, Koonin EV. 2011. Unification of cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol Direct 6:38
16. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNAdirected adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11:181-190
17. Terns MP, Terns RM. 2011. CRISPR-based adaptive immune systems. Curr. Opin. Microbiol. 14:321-327
18. Haft DH, Selengut J, Mongodin EF, Nelson KE. 2005. A guild of 45 CRISPR-associated (cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol. 1:e60. http://dx.doi.org/10.1371/journal.pcbi.0010060
19. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709-1712
20. Edgar R, Qimron U. 2010. The Escherichia coli CRISPR system protects from _ lysogenization, lysogens, and prophage induction. J. Bacteriol. 192:6291-6294
21. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: 1843-1845
22. Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadán AH, Moineau S. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67-71
23. Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O'Toole GA. 2012. The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol. 194:5728-5738
24. Westra ER, Swarts DC, Staals RH, Jore MM, Brouns SJ, van der Oost J. 2012. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311-339
25. Lopez-Sanchez MJ, Sauvage E, Da Cunha V, Clermont D, Ratsima Hariniaina E, Gonzalez-Zorn B, Poyart C, Rosinski-Chupin I, Glaser P. 2012. The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol. Microbiol. 85:1057-1071
26. Louwen R, Horst-Kreft D, de Boer AG, van der Graaf L, de Knegt G, Hamersma M, Heikema AP, Timms AR, Jacobs BC, Wagenaar JA, Endtz HP, van der Oost J, Wells JM, Nieuwenhuis EE, van Vliet AH, Willemsen PT, van Baarlen P, van Belkum A. 2013. A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barré syndrome. Eur. J. Clin. Microbiol. Infect. Dis. 32: 207-226
27. Nam KH, Haitjema C, Liu X, Ding F, Wang H, DeLisa MP, Ke A. 2012. Cas5d protein processes pre-crRNA and assembles into a cascadelike interference complex in subtype I-C/Dvulg CRISPR-Cas system. Structure 20:1574-1584
28. Bikard D, Hatoum-Aslan A, Mucida D, Marraffini LA. 2012. CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection. Cell Host Microbe 12:177-186
29. Al-Attar S, Westra ER, van der Oost J, Brouns SJ. 2011. Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes. Biol. Chem. 392:277-289
30. van der Oost J, Brouns SJ. 2009. RNAi: prokaryotes get in on the act. Cell 139:863-865
31. Tyson GW, Banfield JF. 2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ. Microbiol. 10:200-207
32. Hale C, Kleppe K, Terns RM, Terns MP. 2008. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 14:2572-2579
33. Lillestøl RK, Shah SA, Brügger K, Redder P, Phan H, Christiansen J, Garrett RA. 2009. CRISPR families of the crenarchaeal genus Sulfolobus: bidirectional transcription and dynamic properties. Mol. Microbiol. 72: 259-272
34. Semenova E, Nagornykh M, Pyatnitskiy M, Artamonova II, Severinov K. 2009. Analysis of CRISPR system function in plant pathogen Xanthomonas oryzae. FEMS Microbiol. Lett. 296:110-116
35. Pougach K, Semenova E, Bogdanova E, Datsenko KA, Djordjevic M, Wanner BL, Severinov K. 2010. Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol. Microbiol. 77:1367-1379
36. Hatoum-Aslan A, Maniv I, Marraffini LA. 2011. Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc. Natl. Acad. Sci. U. S. A. 108:21218-21222
37. Hale CR, Majumdar S, Elmore J, Pfister N, Compton M, Olson S, Resch AM, Glover CV III, Graveley BR, Terns RM, Terns MP. 2012. Essential features and rational design of CRISPR RNAs that function with the cas RAMP module complex to cleave RNAs. Mol. Cell 45: 292-302
38. Haurwitz RE, Jinek M, Wiedenheft B, Zhou K, Doudna JA. 2010. Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329:1355-1358
39. Wiedenheft B, Lander GC, Zhou K, Jore MM, Brouns SJ, van der Oost J, Doudna JA, Nogales E. 2011. Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477:486-489
40. Wiedenheft B, van Duijn E, Bultema JB, Waghmare SP, Zhou K, Barendregt A, Westphal W, Heck AJ, Boekema EJ, Dickman MJ, Doudna JA. 2011. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. U. S. A. 108:10092-10097
41. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER, Wanner B, van der Oost J, Brouns SJ, Severinov K. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc. Natl. Acad. Sci. U. S. A. 108: 10098-10103
42. Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, Graham S, Reimann J, Cannone G, Liu H, Albers SV, Naismith JH, Spagnolo L, White MF. 2012. Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol. Cell 45:303-313
43. Wiedenheft B, Zhou K, Jinek M, Coyle SM, Ma W, Doudna JA. 2009. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17:904-912
44. Han D, Lehmann K, Krauss G. 2009. SSO1450-a CAS1 protein from Sulfolobus solfataricus P2 with high affinity forRNAand DNA. FEBS Lett. 583:1928-1932
45. Beloglazova N, Brown G, Zimmerman MD, Proudfoot M, Makarova KS, Kudritska M, Kochinyan S, Wang S, Chruszcz M, Minor W, Koonin EV, Edwards AM, Savchenko A, Yakunin AF. 2008. A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. J. Biol. Chem. 283: 20361-20371
46. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV. 2006. A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1:7
47. Zhang J, Kasciukovic T, White MF. 2012. The CRISPR associated protein Cas4 is a 5= to 3= DNA exonuclease with an iron-sulfur cluster. PLoS One 7:e47232. http://dx.doi.org/10.1371/journal.pone.0047232
48. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471: 602-607
49. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816-821
50. Cady KC, O'Toole GA. 2011. Non-identity-mediated CRISPRbacteriophage interaction mediated via the Csy and Cas3 proteins. J. Bacteriol. 193:3433-3445
51. Carte J, Pfister NT, Compton MM, Terns RM, Terns MP. 2010. Binding and cleavage of CRISPR RNA by Cas6. RNA 16:2181-2188
52. Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O'Toole GA. 2009. Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J. Bacteriol. 191:210-219
53. Deng L, Kenchappa CS, Peng X, She Q, Garrett RA. 2012. Modulation of CRISPR locus transcription by the repeat-binding protein Cbp1 in Sulfolobus. Nucleic Acids Res. 40:2470-2480
54. Richter H, Zoephel J, Schermuly J, Maticzka D, Backofen R, Randau L. 2012. Characterization of CRISPR RNA processing in Clostridium thermocellum and Methanococcus maripaludis. Nucleic Acids Res. 40: 9887-9896
55. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Soria E. 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:174-182
56. Takeuchi N, Wolf YI, Makarova KS, Koonin EV. 2012. Nature and intensity of selection pressure on CRISPR-associated genes. J. Bacteriol. 194:1216-1225
57. Newton HJ, Ang DK, van Driel IR, Hartland EL. 2010. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin. Microbiol. Rev. 23:274-298
58. Fields BS, Benson RF, Besser RE. 2002. Legionella and legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 15:506-526
59. for Disease Control and Prevention, Centers. 2011. Legionellosis- United States, 2000 -2009. MMWR Morb. Mortal. Wkly. Rep. 60: 1083-1086
60. Valster RM, Wullings BA, van den Berg R, van der Kooij D. 2011. Relationships between free-living protozoa, cultivable Legionella spp., and water quality characteristics in three drinking water supplies in the Caribbean. Appl. Environ. Microbiol. 77:7321-7328
61. Lau HY, Ashbolt NJ. 2009. The role of biofilms and protozoa in Legionella pathogenesis: implications for drinking water. J. Appl. Microbiol. 107:368-378
62. Taylor M, Ross K, Bentham R. 2009. Legionella, protozoa, and biofilms: interactions within complex microbial systems. Microb. Ecol. 58: 538-547
63. Buse HY, Schoen ME, Ashbolt NJ. 2012. Legionellae in engineered systems and use of quantitative microbial risk assessment to predict exposure. Water Res. 46:921-933
64. Hsu BM, Huang CC, Chen JS, Chen NH, Huang JT. 2011. Comparison of potentially pathogenic free-living amoeba hosts by Legionella spp. in substrate-associated biofilms and floating biofilms from spring environments. Water Res. 45:5171-5183
65. Swanson MS, Hammer BK. 2000. Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54:567-613
66. Isberg RR, O'Connor TJ, Heidtman M. 2009. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat. Rev. Microbiol. 7:13-24
67. D'Auria G, Jiménez-Hernández N, Peris-Bondia F, Moya A, Latorre A. 2010. Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11:181
68. Faucher SP, Shuman HA. 2011. Small regulatory RNA and Legionella pneumophila. Front Microbiol. 2:98
69. Ginevra C, Jacotin N, Diancourt L, Guigon G, Arquilliere R, Meugnier H, Descours G, Vandenesch F, Etienne J, Lina G, Caro V, Jarraud S. 2012. Legionella pneumophila sequence type 1/Paris pulsotype subtyping by spoligotyping. J. Clin. Microbiol. 50:696-701
70. Grissa I, Vergnaud G, Pourcel C. 2007. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 35:W52-W57
71. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. 2011. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res. 39:9275-9282
72. Molofsky AB, Swanson MS. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40
73. Nam KH, Ding F, Haitjema C, Huang Q, Delisa MP, Ke A. 2012. Double-stranded endonuclease activity in Bacillus halodurans clustered regularly interspaced short palindromic repeats (CRISPR)-associated Cas2 protein. J. Biol. Chem. 287:35943-35952
74. Babu M, Beloglazova N, Flick R, Graham C, Skarina T, Nocek B, Gagarinova A, Pogoutse O, Brown G, Binkowski A, Phanse S, Joachimiak A, Koonin EV, Savchenko A, Emili A, Greenblatt J, Edwards AM, Yakunin AF. 2011. A dual function of the CRISPR-Cas system in bacterial antivirus immunity and DNA repair. Mol. Microbiol. 79:484-502
75. Lammertyn E, Vande Voorde J, Meyen E, Maes L, Mast J, Anné J. 2008. Evidence for the presence of Legionella bacteriophages in environmental water samples. Microb. Ecol. 56:191-197
76. Gomez-Valero L, Rusniok C, Buchrieser C. 2009. Legionella pneumophila: population genetics, phylogeny and genomics. Infect. Genet. Evol. 9:727-739
77. Perez-Rodriguez R, Haitjema C, Huang Q, Nam KH, Bernardis S, Ke A, DeLisa MP. 2011. Envelope stress is a trigger of CRISPR RNAmediatedDNAsilencing in Escherichia coli. Mol. Microbiol. 79:584-599
78. Raivio T. 2011. Identifying your enemies-could envelope stress trigger microbial immunity? Mol. Microbiol. 79:557-561
79. Plagens A, Tjaden B, Hagemann A, Randau L, Hensel R. 2012. Characterization of the CRISPR/Cas subtype I-A system of the hyperthermophilic crenarchaeon Thermoproteus tenax. J. Bacteriol. 194:2491-2500
80. Palmer KL, Whiteley M. 2011. DMS3-42: the secret to CRISPRdependent biofilm inhibition in Pseudomonas aeruginosa. J. Bacteriol. 193:3431-3432
81. Viswanathan P, Murphy K, Julien B, Garza AG, Kroos L. 2007. Regulation of dev, an operon that includes genes essential for Myxococcus xanthus development and CRISPR-associated genes and repeats. J. Bacteriol. 189:3738-3750
82. Aklujkar M, Lovley DR. 2010. Interference with histidyl-tRNA synthetase by a CRISPR spacer sequence as a factor in the evolution of Pelobacter carbinolicus. BMC Evol. Biol. 10:230
83. Maris C, Dominguez C, Allain FH. 2005. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272:2118-2131
84. Samai P, Smith P, Shuman S. 2010. Structure of a CRISPR-associated protein Cas2 from Desulfovibrio vulgaris. Acta Crystallogr. 66: 1552-1556
85. Kang SO, Caparon MG, Cho KH. 2010. Virulence gene regulation by CvfA, a putative RNase: the CvfA-enolase complex in Streptococcus pyogenes links nutritional stress, growth-phase control, and virulence gene expression. Infect. Immun. 78:2754-2767
86. Schroeder GN, Petty NK, Mousnier A, Harding CR, Vogrin AJ, Wee B, Fry NK, Harrison TG, Newton HJ, Thomson NR, Beatson SA, Dougan G, Hartland EL, Frankel G. 2010. Legionella pneumophila strain 130b possesses a unique combination of type IV secretion systems and novel Dot/Icm secretion system effector proteins. J. Bacteriol. 192: 6001-6016
87. Brüggemann H, Hagman A, Jules M, Sismeiro O, Dillies MA, Gouyette C, Kunst F, Steinert M, Heuner K, Coppée JY, Buchrieser C. 2006. Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell. Microbiol. 8:1228-1240
88. Santic M, Ozanic M, Semic V, Pavokovic G, Mrvcic V, Kwaik YA. 2011. Intra-vacuolar proliferation of F. novicida within H. vermiformis. Front Microbiol. 2:78
89. Stewart CR, Burnside DM, Cianciotto NP. 2011. The surfactant of Legionella pneumophila is secreted in a TolC-dependent manner and is antagonistic toward other Legionella species. J. Bacteriol. 193:5971-5984
90. Chatfield CH, Mulhern BJ, Burnside DM, Cianciotto NP. 2011. Legionella pneumophila LbtU acts as a novel, TonB-independent receptor for the legiobactin siderophore. J. Bacteriol. 193:1563-1575
91. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA. 2008. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70:611-625
92. Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40
93. Koo JT, Alleyne TM, Schiano CA, Jafari N, Lathem WW. 2011. Global discovery of small RNAs in Yersinia pseudotuberculosis identifies Yersinia-specific small, noncoding RNAs required for virulence. Proc. Natl. Acad. Sci. U. S. A. 108:709-717
94. Faucher SP, Mueller CA, Shuman HA. 2011. Legionella pneumophila transcriptome during intracellular multiplication in human macrophages. Front Microbiol. 2:60
95. Broich M, Rydzewski K, McNealy TL, Marre R, Flieger A. 2006. The global regulatory proteins LetA and RpoS control phospholipase A, lysophospholipase A, acyltransferase, and other hydrolytic activities of Legionella pneumophila JR32. J. Bacteriol. 188:1218-1226
96. Doléans-Jordheim A, Akermi M, Ginevra C, Cazalet C, Kay E, Schneider D, Buchrieser C, Atlan D, Vandenesch F, Etienne J, Jarraud S. 2006. Growth-phase-dependent mobility of the lvh-encoding region in Legionella pneumophila strain Paris. Microbiology 152:3561-3568
97. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta delta C(T)) method. Methods 25:402-408
98. McCoy-Simandle K, Stewart CR, Dao J, Debroy S, Rossier O, Bryce PJ, Cianciotto NP. 2011. Legionella pneumophila type II secretion dampens the cytokine response of infected macrophages and epithelia. Infect. Immun. 79:1984-1997
99. Charpentier X, Kay E, Schneider D, Shuman HA. 2011. Antibiotics and UV radiation induce competence for natural transformation in Legionella pneumophila. J. Bacteriol. 193:1114-1121
100. Knudson GB. 1985. Photoreactivation of UV-irradiated Legionella pneumophila and other Legionella species. Appl. Environ. Microbiol. 49: 975-980
101. Courcelle J, Crowley DJ, Hanawalt PC. 1999. Recovery of DNA replication in UV-irradiated Escherichia coli requires both excision repair and recF protein function. J. Bacteriol. 181:916-922
102. Al-Deib AA, Mahdi AA, Lloyd RG. 1996. Modulation of recombination and DNA repair by the RecG and PriA helicases of Escherichia coli K-12. J. Bacteriol. 178:6782-6789
103. Yoshida S, Mizuguchi Y. 1984. Antibiotic susceptibility of Legionella pneumophia Philadelphia-1 in cultured guinea-pig peritoneal macrophages. J. Gen. Microbiol. 130:901-906
104. Robey M, O'Connell W, Cianciotto NP. 2001. Identification of Legionella pneumophila rcp, a pagP-like gene that confers resistance to cationic antimicrobial peptides and promotes intracellular infection. Infect. Immun. 69:4276-4286
105. Hazan R, Sat B, Engelberg-Kulka H. 2004. Escherichia coli mazEFmediated cell death is triggered by various stressful conditions. J. Bacteriol. 186:3663-3669.